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Polyols and UV‐Sunscreens in the Prasiola‐Clade (Trebouxiophyceae

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Polyols and UV‐Sunscreens in the Prasiola‐Clade (Trebouxiophyceae J. Phycol. 54, 264–274 (2018) © 2018 The Authors Journal of Phycology published by Wiley Periodicals, Inc. on behalf of Phycological Society of America This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. DOI: 10.1111/jpy.12619 POLYOLS AND UV-SUNSCREENS IN THE PRASIOLA-CLADE (TREBOUXIOPHYCEAE, CHLOROPHYTA) AS METABOLITES FOR STRESS RESPONSE AND CHEMOTAXONOMY1 Vivien Hotter, Karin Glaser Institute of Biological Sciences, Applied Ecology and Phycology, University of Rostock, Albert-Einstein-Straße 3, D-18059 Rostock, Germany Anja Hartmann, Markus Ganzera Institute of Pharmacy, Pharmacognosy, University of Innsbruck, Innrain 80-82/IV, A-6020 Innsbruck, Austria and Ulf Karsten 2 Institute of Biological Sciences, Applied Ecology and Phycology, University of Rostock, Albert-Einstein-Straße 3, D-18059 Rostock, Germany In many regions of the world, aeroterrestrial green algae of the Trebouxiophyceae (Chlorophyta) In contrast to their aquatic relatives, aeroterres- represent very abundant soil microorganisms, and trial algae are directly exposed to the atmosphere hence their taxonomy is crucial to investigate their and thereby subject to harsh environmental condi- physiological performance and ecological impor- tions, such as strong diurnal and seasonal changes tance. Due to a lack in morphological features, of ultraviolet radiation (UVR; Hartmann et al. taxonomic and phylogenetic studies of Treboux- 2016) and strong differences between cellular and iophycean algae can be a challenging task. Since atmospheric water potential (Holzinger and Karsten chemotaxonomic markers could be a great assistance 2013). Differences in water potential drive water in this regard, 22 strains of aeroterrestrial Treboux- movement across membranes, between different cel- iophyceae were chemically screened for their polyol- lular compartments, and between organisms and patterns as well as for mycosporine-like amino acids their environment (e.g., Larcher 2003), and thus (MAAs) in their aqueous extracts using RP-HPLC and determine, for example, water availability for poik- LC-MS. D-sorbitol was exclusively detected in ilohydric organisms, such as green algae (Kranner members of the Prasiolaceae family. The novel MAA et al. 2008). Due to the incapability of green algae prasiolin and a related compound (“prasiolin-like”) to actively regulate the water budget, their cells des- were present in all investigated members of the iccate if the extracellular water potential is lower Prasiola-clade, but missing in all other tested than the intracellular one. Since life without water Trebouxiophyceae. While prasiolin could only be is impossible, uncontrolled dehydration leads to detected in field material directly after extraction, the increasing mortality unless an organism is desicca- “prasiolin-like” compound present in the other algae tion tolerant. In arid regions water is scarce and its was fully converted into prasiolin after 24 h. These availability unpredictable. Nevertheless, many mem- findings suggest D-sorbitol and prasiolin-like com- bers of the Chlorophyta and Streptophyta such as pounds are suitable chemotaxonomic markers for the Interfilum, Klebsormidium, Coccomyxa, Rosenvingiella,or Prasiolaceae and Prasiola-clade, respectively. Addi- Prasiola are found in various terrestrial habitats all tional UV-exposure experiments with selected strains over the world, from deserts and alpine regions to show that MAA formation and accumulation can be urban areas, where they inhabit both natural and induced, supporting their role as UV-sunscreen. artificial surfaces such as soil, tree bark, roof tiles, etc. (e.g., Karsten et al. 2007a,b,c, Rindi 2007, Key index words: chemotaxonomy; MAAs; polyols; Moniz et al. 2012, Darienko et al. 2015, Rysanek prasiolin; sunscreen; terrestrial algae; UV radiation et al. 2015, and references therein). Abbreviations: MAAs, mycosporine-like amino acids; Aeroterrestrial green algae developed numerous RP-HPLC, reversed phase high performance liquid mechanisms to survive desiccation (for review see chromatography; UVR, ultraviolet radiation Holzinger and Karsten 2013). Green algal members of the class Trebouxiophyceae are capable of synthe- 1Received 24 July 2017. Accepted 7 January 2018. First Published sizing and accumulating polyols. These low molecu- Online 18 January 2018. Published Online 21 February 2018, Wiley lar weight carbohydrates exhibit multiple functions. Online Library (wileyonlinelibrary.com). They act as antioxidants, stabilize proteins under 2Author for correspondence: e-mail [email protected]. Editorial Responsibility: W. Henley (Associate Editor) heat stress conditions and are rapidly available 264 CHEMOTAXONOMY IN THE PRASIOLA-CLADE 265 respiratory substrates in case of energy deficiency Prasiola stipitata, but also proved its inducibility by (Yancey 2005, Karsten et al. 2007c). Polyols are also UV exposure. A chemical screening of various mem- osmotically active, that is, they decrease the intracel- bers of the Trebouxiophyceae confirmed the occur- lular water potential when accumulated (Holzinger rence of this 324 nm-MAA in Watanabea spp. and and Karsten 2013). Thereby, desiccation is reduced Prasiola spp. (Karsten et al. 2005, 2007b). Recently, or even prevented without negatively affecting meta- Hartmann et al. (2016) elucidated the chemical bolic integrity. Hence, polyols are also called com- structure of this putative 324 nm-MAA in the closely patible solutes (Yancey 2005). Aeroterrestrial related Prasiola calophylla as N-[5,6 hydroxy-5(hydro- members of the Trebouxiophyceae, such as Apatococ- xymethyl)-2-methoxy-3-oxo-1-cycohexen-1-yl] glu- cus, Chloroidium, Coccomyxa, Prasiola, Rosenvingiella, tamic acid, which indeed represents a novel MAA. It Stichococcus and Trentepohlia, synthesize a variety of was named prasiolin. However, so far only a few polyols, such as arabitol, erythritol, glycerol, ribitol, members of the Trebouxiophyceae have been stud- D-sorbitol and volemitol (Feige and Kremer 1980, ied for the presence of this and other MAAs and Gustavs et al. 2010, 2011). While in some clades like until now the occurrence of prasiolin is experimen- Apatococcus spp. a combination of these substances tally proven only in P. calophylla. can be detected, others like Prasiola spp. contain Stress metabolites such as polyols and MAAs are only one compound (Gustavs et al. 2011). There- not only essential for the long-term survival of green fore, polyol and other low molecular weight carbo- algae under atmospheric conditions, but they can hydrate patterns can be used for chemotaxonomy also be useful in chemotaxonomy. Many aeroterres- (Karsten et al. 1999). trial green algae resemble each other morphologi- Throughout the day or season, exposure to UVR cally (Rindi 2007) and some species even display can change rapidly. While UV-C (200–280 nm) is high phenotypic plasticity (Rindi and Guiry 2002, biologically irrelevant as this wavelength is absorbed Darienko et al. 2015, 2016). This makes green algal by the ozone layer of the stratosphere, both UV-A identification down to the species level based on (315–400 nm) and UV-B (280–315 nm) reach earth’ morphological traits often complicated and some- surface. UV-B radiation is especially harmful to times even unreliable (John and Maggs 1997, Rindi many biological processes (McKenzie et al. 2007, 2007). Polyphasic approaches combining morpho- and references therein), such as photosynthesis or logical, molecular and/or physiological/biochemical enzyme activity (Holzinger and Lutz€ 2006, Sharma data sets are a promising solution to overcome these et al. 2017, and references therein). Since photosyn- problems in species identification (Proeschold and thesis is a physiological key process for algae, its Leliaert 2007, Coesel and Krienitz 2008, Darienko function is vital. et al. 2010). To oppose UVR damage, aeroterrestrial Treboux- In chemotaxonomy, chemical traits are used to iophyceae belonging to the Lobosphaera-, Watanabea- assign organisms to taxa with equal compounds. and Prasiola-clade biosynthesize and accumulate Any chemical compound is suitable as a chemotaxo- mycosporine-like amino acids (MAAs; Karsten et al. nomic marker if it is taxon specific, consistent 2005, 2007b). These sunscreen compounds absorb within a lineage and present in detectable amounts UVR and re-emit it as harmless heat, thereby shield- (Karsten et al. 2007a). Prominent examples are pho- ing intracellular structures and biomolecules (Ban- tosynthetic pigments for algae subdivision (Roy daranayake 1998). MAAs are the most common et al. 2011) or low-molecular weight carbohydrate photoprotective compounds in aquatic organisms, patterns to distinguish lineages within the Bangio- from cyanobacteria and algae to invertebrates and phyceae (Karsten et al. 1999). Stress metabolites can fish (Dunlap and Shick 1998, Sommaruga and Gar- also be suitable chemotaxonomic markers (Dar- cia-Pichel 1999). While MAAs have been investigated ienko et al. 2010). Gustavs et al. (2011) screened a extensively in red algae (Karsten et al. 1998, Frank- wide range of Trebouxiophyceae for their polyols lin et al. 1999, Karsten and Wiencke 1999, Karsten and detected several clade-specific patterns. For 2000, Kr€abs et al. 2002, Boedeker and Karsten 2005, instance, D-sorbitol was proposed as a marker for Pandey et al. 2017) as well as in cyanobacteria and the Prasiola-, D-ribitol for
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